Acceptability of and barriers to human papillomavirus vaccination in China: A systematic review of the Chinese and English scientific literature
2022; Wiley; Volume: 31; Issue: 3 Linguagem: Inglês
10.1111/ecc.13566
ISSN1365-2354
AutoresDu Wang, Jing Wu, Jianshu Du, Haley Ong, Biwei Tang, Marshall Dozier, David Weller, Christine Campbell,
Tópico(s)Hepatitis B Virus Studies
ResumoEuropean Journal of Cancer CareEarly View e13566 ORIGINAL ARTICLEOpen Access Acceptability of and barriers to human papillomavirus vaccination in China: A systematic review of the Chinese and English scientific literature Du Wang, Corresponding Author Du Wang duwang84@163.com orcid.org/0000-0003-1464-1733 Usher Institute, Teviot Place, University of Edinburgh, Edinburgh, UK The George Institute for Global Health, Peking University Health Science Center, Beijing, China Correspondence Du Wang and Christine Campbell, Usher Institute, University of Edinburgh, Edinburgh, EH8 9AG, UK. Email: duwang84@163.com; Christine.Campbell@ed.ac.ukSearch for more papers by this authorJing Wu, Jing Wu National Center for Chronic and Non-communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, ChinaSearch for more papers by this authorJianshu Du, Jianshu Du Ordos Central Hospital, Ordos, ChinaSearch for more papers by this authorHaley Ong, Haley Ong Usher Institute, Teviot Place, University of Edinburgh, Edinburgh, UKSearch for more papers by this authorBiwei Tang, Biwei Tang Shenzhen Nanshan Center for Chronic Disease Control, Shenzhen, ChinaSearch for more papers by this authorMarshall Dozier, Marshall Dozier College Lead for Library Academic Support, Medicine & Veterinary Medicine Library & University, University of Edinburgh, Edinburgh, UKSearch for more papers by this authorDavid Weller, David Weller Usher Institute, Teviot Place, University of Edinburgh, Edinburgh, UKSearch for more papers by this authorChristine Campbell, Corresponding Author Christine Campbell Christine.Campbell@ed.ac.uk Usher Institute, Teviot Place, University of Edinburgh, Edinburgh, UK Correspondence Du Wang and Christine Campbell, Usher Institute, University of Edinburgh, Edinburgh, EH8 9AG, UK. Email: duwang84@163.com; Christine.Campbell@ed.ac.ukSearch for more papers by this author Du Wang, Corresponding Author Du Wang duwang84@163.com orcid.org/0000-0003-1464-1733 Usher Institute, Teviot Place, University of Edinburgh, Edinburgh, UK The George Institute for Global Health, Peking University Health Science Center, Beijing, China Correspondence Du Wang and Christine Campbell, Usher Institute, University of Edinburgh, Edinburgh, EH8 9AG, UK. Email: duwang84@163.com; Christine.Campbell@ed.ac.ukSearch for more papers by this authorJing Wu, Jing Wu National Center for Chronic and Non-communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, ChinaSearch for more papers by this authorJianshu Du, Jianshu Du Ordos Central Hospital, Ordos, ChinaSearch for more papers by this authorHaley Ong, Haley Ong Usher Institute, Teviot Place, University of Edinburgh, Edinburgh, UKSearch for more papers by this authorBiwei Tang, Biwei Tang Shenzhen Nanshan Center for Chronic Disease Control, Shenzhen, ChinaSearch for more papers by this authorMarshall Dozier, Marshall Dozier College Lead for Library Academic Support, Medicine & Veterinary Medicine Library & University, University of Edinburgh, Edinburgh, UKSearch for more papers by this authorDavid Weller, David Weller Usher Institute, Teviot Place, University of Edinburgh, Edinburgh, UKSearch for more papers by this authorChristine Campbell, Corresponding Author Christine Campbell Christine.Campbell@ed.ac.uk Usher Institute, Teviot Place, University of Edinburgh, Edinburgh, UK Correspondence Du Wang and Christine Campbell, Usher Institute, University of Edinburgh, Edinburgh, EH8 9AG, UK. Email: duwang84@163.com; Christine.Campbell@ed.ac.ukSearch for more papers by this author First published: 01 March 2022 https://doi.org/10.1111/ecc.13566AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Abstract Introduction Widespread adoption of the human papillomavirus (HPV) vaccine will require population acceptance and tailoring of immunisation services to community needs and preferences. We examined peer-reviewed publications on the acceptability of and barriers to the HPV vaccine across China. Methods We searched English (MEDLINE, Embase, and Web of Science) and Chinese (CNKI, VIP, Wanfang data) databases between 1 January 2006 and 31 December 2017. We adopted a narrative approach for data synthesis. Results We identified 73 studies. The overall median acceptability of HPV vaccine was 71.8% (Q1–Q3: 58.6%–81%). Low levels of acceptability ( 90%) and urban eastern regions (all <35%). Despite these regional variations, common barriers to HPV vaccine acceptance were concerns about vaccine safety, uncertainty over vaccine effectiveness, low perceived risk of cervical cancer and the price of the vaccine. The level of willingness to pay for the HPV vaccine (over 153 US dollars) was very low (<7%). Conclusion The acceptability of and attitudes towards HPV vaccine vary by regions and populations across China. HPV vaccination programmes will need to tailor service delivery as well as information materials to take account of regional concerns. 1 INTRODUCTION Cervical cancer is the second most common cancer in women aged 15–44 years in China, with an estimated 106,430 new cases and 47,739 deaths occurring annually (Bruni et al., 2018, 2019). The annual increase of incidence and mortality of cervical cancer was the second highest among female cancers in the decade from 2000 to 2011 (Chen et al., 2016; Hu, Zheng, et al., 2014b). In 2018, the World Health Organization (WHO) launched a global strategy towards the elimination of cervical cancer and set three targets for the year 2030—‘90% coverage of HPV vaccination, 70% coverage of twice-lifetime screening, and 90% access to cervical precancer and cancer treatment services and palliative care’ (Canfell et al., 2020). China's National Health Commission (NHC) has given full support to the WHO's global strategy. The Chinese Government's policy document Health China 2030—signalling the government's commitment to investing in health—included fast-tracking conditional approval of the nine-valent HPV vaccine and removing import tariffs on cancer drugs (F. Zhao & Qiao, 2019). Imported vaccines against Human Papilloma Virus—Cervarix (bivalent vaccine) and Gardasil (quadrivalent and nine-valent vaccine)—were approved in China in 2016 (Pan et al., 2016), 2017(Yin, 2017) and 2018(Lin et al., 2019), respectively (Cao, 2020; Yin, 2017). A domestic vaccine—Cecolin—was approved in January 2020, with a two-dose schedule for adolescents aged 9–14 years, and three doses for females aged 15–45 years (Cao, 2020). In May 2020, Cecolin obtained WHO pre-qualification and was approved by the National Medical Products Administration (NMPA) for shipment of 100,000 doses to mainland China. However, the sole vaccine supply is inadequate to meet demand. Current government policy (Cao, 2020; Y. Xue, 2019) is that individuals can self-pay for the HPV vaccine through their private or employer insurance (Cao, 2020; Y. Xue, 2019)—a decision that may be determined by an individual perceptions of the HPV vaccine. A review of the global literature has suggested that women's choices over use of the HPV vaccine are influenced by multiple factors including the cost of vaccination, perceived efficacy and safety of the vaccine, and provision of information about vaccination (Santhanes et al., 2018). Concerns about the safety and effectiveness of the HPV vaccine in China have been influenced by media reports of vaccine safety incidents between 2013 and 2018(Hu et al., 2020; J. Ren et al., 2018; Yang et al., 2014). There is little evidence to support these concerns; however it has been difficult to assuage public doubts about HPV vaccination. Population characteristics affect acceptability; Lin et al. (2019) and You et al. (2020) reported socio-economic status was associated with a willingness to accept imported HPV vaccines among female undergraduates in China. A subsequent study in Shanghai reported migrants had lower confidence in the vaccine's benefits compared with the urban population, but were not as concerned about safety issues (J. Ren et al., 2018). Despite an increasing focus on attitudes towards and acceptability of HPV vaccination in China, there is a dearth of comprehensive analysis, and limited data on any variation by demography or geography. To date, only one systematic review and meta-analysis (Y. Zhang et al., 2016) has been published on the knowledge and acceptability of the HPV vaccine among Chinese populations. The pooled acceptability of the HPV vaccine was 67.25%, with rates varied by sex, ethnicity and geographic regions. Safety of the vaccine was the main concern raised (Y. Zhang et al., 2016). However, variations of attitudes by region and socio-economic status of populations were not explored. The most recent and comprehensive survey among the Chinese population was a multicenter research study in 136 universities across eastern (78), central (27) and western (31) regions of China in 2019 (You et al., 2020). This study reported moderate acceptance (54%) of the HPV vaccine—the proportion of the sampled population who say they would be willing to receive the HPV vaccine. Living in central and western regions and low socio-economic status were found to be associated with low levels of willingness to receive the HPV vaccination (You et al., 2020). However, barriers were not presented in terms of regional or socio-economic status (You et al., 2020). We have carried out a systematic literature review of the acceptability of the HPV vaccine, and attitudes influencing the uptake of the HPV vaccine, across in the three regions (eastern, central and western) of China, and also reporting on variations in attitudes and acceptability by heterogeneous population groups, in order to inform targeted education strategies. 2 MATERIALS AND METHODS 2.1 Search strategy and selection criteria We searched English-language databases: MEDLINE, Embase, and Web of Science and Chinese-language databases: China National Knowledge Infrastructure (CNKI), VIP Database for Chinese Technical Periodicals (VIP) and Wanfang data for relevant articles published between 1 January 2006 and 31 December 2017. The search terms are provided in Table S1. We included research studies if they included Chinese populations, assessed the acceptability of HPV vaccine and factors that may affect this level and were carried out in Mainland China, not in Hong Kong, Macao and Taiwan. Studies were excluded if they did not present original data (e.g., review), outcomes were not completely presented preventing data extraction, or only reported data on either knowledge or awareness of HPV and vaccine but did not report on acceptability and attitudes. The study selection followed Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines (Moher et al., 2009) and the selection process is displayed in Figure 1. FIGURE 1Open in figure viewerPowerPoint Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow diagram for selection of studies DuW, JD and BT independently reviewed the titles and abstracts in the Chinese databases. HO and DuW reviewed the English titles and abstracts. Disagreement on the records were discussed and clarified by DuW. The final decision was made by DuW for the inclusion of articles in the systematic review. 2.2 Data synthesis A standardised data extraction form was used (variables included study date, setting, participant characteristics, and the outcomes of each study). When identifying reported reasons for not accepting the HPV vaccine, we extracted the exact wording from English published papers, and translated Chinese wording into English from Chinese published papers. Four authors (DuW, HO, JD and BT) extracted the information from included studies and any disagreements were resolved through discussion. Study populations described in more than one paper were included as one research study, with any duplicate data excluded. An adapted version of Zaza's validated checklist (Zaza et al., 2000) (Table S2) was used to assess the quality of included studies. The checklist was translated from English into Chinese for quality assessment of the Chinese language studies, and assessed according to the checklist by three authors (DuW, JD and BT). Studies in English were assessed by HO and DuW; disagreements were resolved through discussion. Each study was graded as ‘good’, ‘fair’ or ‘low’ quality based on the scores generated by Zaza's checklist (Zaza et al., 2000). The outcome was presented in the Quality Assessment Tables (Table S3). ‘Low’ quality studies were removed for data synthesis. A narrative approach was used to synthesise data (Ryan & Cochrane Consumers and Communication Review Group, 2020). Given the heterogeneity between studies (e.g., geographical regions, study populations and methods), and analytical strategies (adjustment for different confounders), meta-analysis of data was not feasible. The rationale for using narrative synthesis instead of meta-analysis is summarised in Table S4. We reported HPV vaccine acceptability and reasons for not taking HPV vaccine among people across geographical regions (eastern, central and western China). Table S5 summaries socio-demographic characteristics of the regions in China. The full results from each study, including stratification by rurality, by gender, by population subgroups (i.e., undergraduates, parents and medical providers) were summarised in supplementary materials, grouped according to whether studies presented acceptability for oneself, or for a daughter or son, willingness to pay for the HPV vaccine by price ranges, and the reasons for not accepting the HPV vaccine. We used box plots to describe regional variation. For each region, we presented summary figures (the median with the first quantile and the third quantile) showing the acceptability of the HPV vaccine by rural/urban residence, and gender. For studies reporting results on reasons to accept or decline the HPV vaccine, we extracted the exact wording of reasons from English language papers and translated the wording of reasons into English from Chinese language papers and then summarised the results by multiple/single choice answers, populations and region. There was sufficient similarity in wording across studies to allow collation and comparison of findings. For studies reporting results of acceptability variation by the price of the vaccine, we extracted data that provided the acceptability by price ranges (i.e., under 15.3(¥100), 15.3–45.9(¥300), 45.9–76.5 (¥500), 76.5–153(¥1,000), and over 153 US dollars), grouping data by the lowest threshold of paying for the HPV vaccine (<3.06(¥20), <7.65(¥50), <15.3, <45.9, 15.3, >153 US dollars). For studies exploring acceptability of domestic versus imported vaccines, we summarised the result by the most commonly used price range ( 76.5 US dollars). The protocol of this study is registered with PROSPERO, number CRD42018085894. R software (version 3.5.2; https://www.r-project.org/) was used for descriptive analysis. 3 RESULTS 3.1 Characteristics of included studies A total of 1062 records from Chinese language and 266 from English language searches were identified. Seventy-three studies (56 Chinese language and 17 English language), covering 24 provincial regions across mainland China and presenting data for 110,754 individuals, were selected for inclusion in the review (Figure 1). The characteristics and results of the studies are summarised in Tables 1 and S6. All 73 included studies used a cross-sectional survey approach. The median sample size was 757 participants (range 104–13,024), with the majority of studies (73, 80.2%) having less than 2000 participants. Articles were published from 2007 to 2017. Many studies examined multiple topics including awareness of HPV, and understanding of the HPV vaccine. We report on acceptability, and barriers influencing acceptability of the vaccine. TABLE 1. Characteristics of included studies Study Region Study setting People Sex Feng SW 2010 (S. Feng et al., 2012) Eastern Rural/urban hospital Rural/urban women outpatients Female Hong Y, 2013 (Hong et al., 2013) Eastern Community Female sex workers Female Zhao FH, 2012 (F. H. Zhao et al., 2012) Mixed Urban/rural hospital General population, government officials and healthcare providers Mixed Zhou YQ 2016 (Y. Q. Zhou, Yang, & Wu, 2016b) Eastern Urban hospital Healthcare providers Female Ma D 2012 (X. J. Ma, Meng, et al., 2013b) Eastern Urban hospital Healthcare providers Mixed Wang HQ 2011 Eastern Urban hospital Healthcare providers NA Gao J 2017 (Gao, Zhen, & Liu, 2017a) Central Urban community Healthcare providers NA Li J 2011(J. Li, 2011) Eastern Rural/urban hospital Healthcare providers and government officials Mixed Fu CJ, 2014(Fu et al., 2014) Western Medical university Medical students Mixed Ma D 2013 (D. Ma, Wei, et al., 2013a) Eastern College Medical students Mixed Gu C, 2015 (Gu et al., 2015) Central Medical university Medical students Female Pan XF, 2014 (Pan et al., 2014) Western Medical university Medical students Mixed Zou H, 2016 (Zou, Meng, et al., 2016a) Eastern Sexual health clinic Men Male Zhang YY 2016 (Y. Y. Zhang, 2016) Eastern School Parents of children Female Zhang SK, 2015 (S. K. Zhang et al., 2015) Mixed Middle school, junior Parents of teenagers Mixed Hu HS 2014 (Hu, Ren, et al., 2014a) Eastern Middle school Parents of teenagers Mixed Zhang H 2014 (H. Zhang, Yu, et al., 2014a) Central School Parents of teenagers Mixed Wang W, 2015 (W. Wang, Ma, et al., 2015b) Eastern Middle school, junior Parents of teenagers Mixed Yu Y, 2016 (Y. Yu et al., 2016) Eastern High school, primary, junior, senior Parents of teenagers Female Yan J 2013 (J. Yan et al., 2013) Western Rural community Rural adult women Female Ye JR 2011 (Ye, 2011) Eastern Rural community Rural adult women Female Zhang XX 2014 (X. X. Zhang, Zhao, et al., 2014c) Eastern Rural hospital Rural adult women Female Cheng Y 2017 (Cheng et al., 2017) Central Rural community Rural adult women Female Song D 2007 (Song, 2007) Central Rural community Rural adult women Female Li J, 2015 (J. Li et al., 2015) Central Villages Rural adult women Female Yu J 2013 (J. Yu et al., 2013) Western Rural/urban community Rural adult women, government officials and healthcare providers Mixed Wang XM 2012 (X. M. Wang et al., 2012) Central Rural community/urban hospital Rural women residents/urban women outpatients Female Cui B 2010 (Cui, 2010) Eastern Rural community/urban hospital Rural women/urban women patients Female Xue L, 2018 (L. Xue et al., 2018) Eastern Middle school, junior Teenagers Mixed Wang SM, 2014 (S. M. Wang, Zhang, et al., 2014a) Mixed University Undergraduate students Mixed Zeng XM 2015 (Zeng et al., 2015) Eastern College Undergraduate students Mixed He X 2010 (X. He et al., 2010) Central College Undergraduate students Mixed Zhu YR 2017 (Y. R. Zhu et al., 2017) Central College Undergraduate students Mixed Zhou Y 2012 (Y. Zhou et al., 2012) Central College Undergraduate students Mixed Gong FQ 2014 (Gong, 2014) Eastern College Undergraduate students Mixed Xu J 2014 (Xu & Li, 2014) Western College Undergraduate students Mixed Yang J 2016 (J. Yang et al., 2016) Western College Undergraduate students Female Zou H, 2016 (Zou, Wang, et al., 2016b) Eastern University Undergraduate students Mixed Huang H 2013 (H. Huang et al., 2013) Western College Undergraduate students Mixed Liu RJ 2017 (R. J. Liu et al., 2017) Eastern College Undergraduate students Mixed Li M 2013 (M. Li et al., 2013) Eastern NA Undergraduate students and parents of teenagers Mixed Liu Q 2015 (Q. Liu et al., 2015) Central College Undergraduate students and parents of teenagers Mixed Lu J 2016 (Lu et al., 2016) Eastern College/urban community/hospital Undergraduate students/government/HCPs Mixed Tian T 2017 (Tian, 2017) Western NA Urban adult men Male Zhu JH 2016 (J. H. Zhu et al., 2016) Eastern Urban CDC Urban adult men Male Huang YH 2014 (Y. H. Huang et al., 2014) Eastern Urban community Urban adult men and women Mixed Li J 2008 (J. Li et al., 2009) Eastern Urban community Urban adult women Female Zhang SK 2014 (S. K. Zhang, Huang, et al., 2014b) Mixed NA Urban adult women Female Lei JH 2015 (Lei & Zhong, 2015) Eastern Urban hospital Urban adult women Female Meng LP 2015 (Meng et al., 2015) Eastern Urban community Urban adult women Female Yang GQ 2013 (G. Q. Yang et al., 2013) Eastern Urban hospital Urban adult women Female Zhou YQ 2016 (Y. Q. Zhou, Yang, & Wu, 2016b) Eastern Urban community Urban adult women Female Ran LM 2014 (Ran et al., 2014) Western Urban hospital Urban adult women Female Liu XW 2016 (X. W. Liu et al., 2016) Eastern Urban hospital Urban adult women Female Ma XJ 2013 (X. J. Ma, Meng, et al., 2013b) Eastern Urban hospital Urban adult women Female Zhao DJ 2010 (D. J. Zhao et al., 2010) Eastern Urban community Urban adult women Female Shao SJ 2013 (Shao et al., 2013) Eastern Urban hospital Urban adult women Female Hu SY, 2011 (S. Y. Hu et al., 2011) Eastern Rural (Binhai), suburban (Jintan) and urban (Xuzhou) Urban and rural women Female Li J, 2009 (J. Li et al., 2009) Mixed Urban community cluster and rural areas Urban and rural women Female Feng S, 2012 (S. Feng et al., 2012) Eastern Urban/rural hospital Urban and rural women Female Wu Y 2011 (Wu, 2011) Eastern NA Urban women adults Female Chang IJ, 2013 (Chang et al., 2013) Mixed Companies and universities Urban women and undergraduate students Female He M 2011 (M. He et al., 2011) Mixed Urban hospital Urban women outpatients/urban hps Female Xiao W 2010 (Xiao & Bian, 2009) Eastern Urban hospital Urban women patients Female Huang GF 2011 (G. F. Huang, 2011) Eastern Urban hospital Urban women patients Female Xie WL 2015 (Xie et al., 2015) Central Urban hospital Urban women patients Female Fan BJ 2009 (Fan, 2009) Eastern Urban hospital Urban women patients Female Su Q 2016 (Su et al., 2016) Western Urban hospital Urban women patients Female Wang X 2014 (X. Wang, Lei, et al., 2014b) Western Urban hospital Urban women patients Female Zhu QY 2015 (Q. Y. Zhu et al., 2015) Eastern Urban hospital Urban women patients Female Fatima 2014 (Fatima, 2014) Western Rural community Uyghur rural adult women Female Ren CL 2011 (C. L. Ren et al., 2011) Western NA Uyghur/Hui/Han women adults Female Wang L 2015 (L. Wang, Ouyang, & Wang, 2015a) Central Urban hospital Medical students Female 3.1.1 Geographical distribution Of the 73 studies, the majority (40) were conducted in eastern China (Guangdong, Beijing, Hebei, Zhejiang, Liaoning, Shandong, Shanghai, Tianjin and Jiangsu), 13 studies in western China (Xinjiang, Yunnan, Chongqing, Shaanxi, Gansu, Inner Mongolia, Guizhou and Sichuan) and 13 in central China (Hunan, Jiangxi, Shanxi, Hubei and Henan). Seven studies were multicenter, recruiting participants across two or three regions of China. Publications from three areas—Beijing, Guangdong and Zhejiang—predominated (27 in total) (Figure 2). FIGURE 2Open in figure viewerPowerPoint Map of mainland China, showing the number of studies in each province and region 3.1.2 Study participants The majority of studies (39 in total) were conducted among adult women, 20 among undergraduate students, seven among parents of teenagers, six among healthcare providers, four among adult men, two among Uyghur people and one among teenagers (aged 11–18 years). Studies examining the views of ethnic minority groups (Uyghur, Mongolian and Hui peoples) were only found from western China (Tables 1 and S6). Most studies (38) were undertaken in urban areas, with 10 in rural areas, and 9 in both urban and rural areas (Table S7). 3.2 Quality of included studies Overall, 23 studies were of ‘good’ quality, 50 were ‘fair’ and 14 were ‘low’ (Table S3). Low quality studies were excluded from data synthesis. Studies carried out in western China were more likely to be of lower quality whereas those reporting data from eastern China were more likely to clearly describe the study population, outcomes, statistical tests and study instruments. Full details are available in Tables S3 and S4. 3.3 Acceptability of the HPV vaccine Fifty-eight studies assessed the level of acceptability of the HPV vaccine. Acceptability of HPV vaccine was generally defined as the proportion of people willing to have HPV vaccine. The overall median rate of acceptability of the HPV vaccine was 71.8% (Q1-Q3: 58.6%–81%). Regional variation was observed: studies from western China reported a higher acceptability (median: 84.7%, Q1–Q3: 74.3%–94.1%) compared with those from eastern China (median: 68.4%, Q1–Q3: 56.8%–76.4%) and central China (median: 59.9%, Q1–Q3: 50.6%–75.5%) (Figure 3). In 52 of 58 studies, the acceptability of the HPV vaccine was over 50% (Table S7). Ten studies reported over 80% baseline acceptability of HPV vaccine (Fan, 2009; Fatima, 2014; Fu et al., 2014; He et al., 2011; Liu et al., 2016; Ren et al., 2011; Tian, 2017; Yan et al., 2013; Zhao et al., 2012). In contrast, eight studies from eastern China reported low levels of acceptability of HPV vaccine (less than 40% willingness) (Hong et al., 2013; Hu, Ren, et al., 2014a; Ma et al., 2012; Ma, Meng, et al., 2013b; Y. Yu et al., 2016; S. K. Zhang et al., 2015; Y. Y. Zhang, 2016; Zou, Meng, et al., 2016a) across various population groups including female sex workers (Hong et al., 2013), healthcare providers (D. Ma et al., 2012), parents of teenagers (Y. Yu et al., 2016; S. K. Zhang et al., 2015; Y. Y. Zhang, 2016) and urban men (Y. H. Huang et al., 2014; Zou, Meng, et al., 2016a) and women (Ma, Meng, et al., 2013b). For example, Yu et al. (2016), Zhang (2016) and Ma, Meng, et al. (2013b) found that 24.7%–33% of respondents indicated that they would be willing to take the HPV vaccine in urban and rural areas of Shandong and Fujian. Ma et al. (2012) found that 25%–37% healthcare providers in urban Hebei indicated a willingness to accept the vaccine. Zhang et al. (2015) found low overall intention of accepting the HPV vaccine (36.2%) in seven provinces in both western and eastern China: however, it is not possible to disaggregate the results by region (S. K. Zhang et al., 2015) (Table S7). FIGURE 3Open in figure viewerPowerPoint Acceptability of human papillomavirus (HPV) vaccine by region When taking account of rurality and regional location, the largest differences in acceptability were observed between rural western and urban eastern groups. For example, Fatima (2014), Yan et al. (2013) and Yu et al. (2013) reported high levels of acceptability of HPV vaccine (exceeding 90%) in rural western China, whereas Yu Y 2016, Zhang YY 2016 and Ma XJ 2013 reported levels of acceptability of HPV vaccine of no more than 35% in urban eastern China (Table S7). Five studies (Fatima, 2014; Fu et al., 2014; Y. H. Huang et al., 2014; Wang, Zhang, et al., 2014a; L. Xue et al., 2018) stratified level of acceptability of the HPV vaccine by gender. In each study, the authors found women were more likely to express a willingness to be vaccinated than men. Two studies among undergraduates found that 73.2%–87.5% of females and 68.3%–81.8% of males would accept the HPV vaccine (Fu et al., 2014; Wang, Zhang, et al., 2014a) (Table S7). Twenty-five studies assessed the level of parental acceptability of the HPV vaccine for a child (Chang et al., 2013; Cui, 2010; Fan, 2009; Fatima, 2014; Fen, 2010; M. He et al., 2011; Hong et al., 2013; Hu, Ren, et al., 2014a; Lei & Zhong, 2015; J. Li, 2011; J. Li et al., 2015; J. Li et al., 2009; M. Li et al., 2013; D. Ma et al., 2012; Pan et al., 2014; C. L. Ren et al., 2011; Su et al., 2016; Wang, Ma, et al., 2015b; Xiao & Bian, 2009; Xie et al., 2015; Zhang, Yu, et al., 2014a; Zhang, Huang, et al., 2014b; S. K. Zhang et al., 2015; Y. Y. Zhang, 2016; Zhao et al., 2010; F. H. Zhao et al., 2012; Zhou, Fan, et al., 2016a; Zou, Wang, et al., 2016b). The majority of studies (19 of 25) reported levels of acceptability of the HPV vaccine for either a daughter or a son exceeded 50%. Seven studies (Fan, 2009; Fatima, 2014; M. He et al., 2011; J. Li, 2011; J. Li et al., 2015; J. Li et al., 2009; C. L. Ren et al., 2011) reported high levels of acceptability of the HPV vaccine (over 80% acceptability). However, it is important to note that many of these studies (19 of 25) were carried out among health care providers, gynaecology patients, or undergraduates, with respondents having either adult daughters or sons, or no children at present. Only six studies were carried out among parents of teenagers: among these studies, the level of acceptability of the HPV vaccine was lower, ranging from 8.2% to 42.8%; (Hu, Ren, et al., 2014a; M. Li et al., 2013; Wang, Ma, et al., 2015b; H. Zhang, Yu, et al., 2014a; S. K. Zhang et al., 2015; Y. Y. Zhang, 2016). One study in Fujian(Y. Y. Zhang, 2016) reported a higher acceptability of 58% for their daughters (Table S8). 3.4 Barriers to uptake of the HPV vaccine Studies reporting
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